The State of Migratory Landbirds in the East Asian Flyway: Distributions, Threats, and Conservation Needs
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
REVIEW
published: 13 April 2021
doi: 10.3389/fevo.2021.613172
The State of Migratory Landbirds in
the East Asian Flyway: Distributions,
Threats, and Conservation Needs
Ding Li Yong 1* , Wieland Heim 2 , Sayam U. Chowdhury 3,4 , Chang-Yong Choi 5 ,
Pavel Ktitorov 6 , Olga Kulikova 6 , Alexander Kondratyev 6 , Philip D. Round 7 ,
Desmond Allen 8 , Colin R. Trainor 9 , Luke Gibson 10 and Judit K. Szabo 9,11
1
BirdLife International (Asia), Tanglin International Centre, Singapore, Singapore, 2 Institute of Landscape Ecology, University
of Münster, Münster, Germany, 3 Bangladesh Spoon-billed Sandpiper Conservation Project, Dhaka, Bangladesh,
4
Conservation Science Group, Department of Zoology, University of Cambridge, Cambridge, United Kingdom, 5 Department
of Agriculture, Forestry, and Bioresources, Seoul National University, Seoul, South Korea, 6 Institute of Biological Problems
of the North, Russian Academy of Sciences, Magadan, Russia, 7 Department of Biology, Faculty of Science, Mahidol
University, Bangkok, Thailand, 8 Streaked Reed Warbler Project, Manila, Philippines, 9 College of Engineering,
IT and Environment, Charles Darwin University, Casuarina, NT, Australia, 10 School of Environmental Science
and Engineering, Southern University of Science and Technology, Shenzhen, China, 11 Programa de Pós-Graduação em
Biodiversidade e Evolução, Instituto de Biologia, Universidade Federal da Bahia, Salvador, Brazil
With nearly 400 migratory landbird species, the East Asian Flyway is the most diverse
of the world’s flyways. This diversity is a consequence of the varied ecological niches
Edited by:
Binbin Li, provided by biomes ranging from broadleaf forests to arctic tundra and accentuated by
Duke Kunshan University, China complex biogeographic processes. The distribution and migration ecology of East Asian
Reviewed by: landbirds is still inadequately known, but a recent explosion in the number of studies
Lei Cao,
Research Center
tracking the migration of raptors, cuckoos, kingfishers and passerines has greatly
for Eco-Environmental Sciences increased our knowledge about the stopover and wintering ecology of many species,
(CAS), China
and the migratory routes that link northeast Eurasia and the Asian tropics. Yet the East
Theunis Piersma,
University of Groningen, Netherlands Asian Flyway also supports the highest number of threatened species among flyways.
*Correspondence: Strong declines have been detected in buntings (Emberizidae) and other long-distance
Ding Li Yong migrants. While the conservation of migratory landbirds in this region has largely focused
dingli.yong@birdlife.org
on unsustainable hunting, there are other threats, such as habitat loss and increased
Specialty section: agro-chemical use driven directly by land cover change and climate-related processes.
This article was submitted to Important knowledge gaps to be addressed include (1) threats affecting species in
Conservation and Restoration
Ecology,
different parts of their annual cycle, (2) range-wide population trends, (3) ecological
a section of the journal requirements and habitat use during the non-breeding season, and (4) the conservation
Frontiers in Ecology and Evolution
status of critical wintering sites (including understudied farming landscapes, such as rice
Received: 01 October 2020
fields) and migration bottlenecks along the flyway.
Accepted: 08 February 2021
Published: 13 April 2021 Keywords: biome, climate change, ecosystem role, habitat loss, hunting, land use change, migration, tracking
Citation:
Yong DL, Heim W,
Chowdhury SU, Choi C-Y, Ktitorov P, INTRODUCTION
Kulikova O, Kondratyev A, Round PD,
Allen D, Trainor CR, Gibson L and The decline of migratory species is a global conservation concern (Wilcove and Wikelski, 2008)
Szabo JK (2021) The State
across the world’s major flyways (Lloyd-Evans and Atwood, 2004; Galbraith et al., 2014; Beresford
of Migratory Landbirds in the East
Asian Flyway: Distributions, Threats,
et al., 2019). Migratory species declines and the associated drivers are well documented for
and Conservation Needs. birds that migrate between North America and the Neotropics (Robinson and Wilcove, 1994;
Front. Ecol. Evol. 9:613172. Lloyd-Evans and Atwood, 2004; Bennett et al., 2018) and for species that breed in Europe
doi: 10.3389/fevo.2021.613172 and winter in Sub-Saharan Africa (Bibby, 1992; Sanderson et al., 2006; Vickery et al., 2014;
Frontiers in Ecology and Evolution | www.frontiersin.org 1 April 2021 | Volume 9 | Article 613172
Yong et al. Conservation of East Asian Landbirds
Beresford et al., 2019), but less so for other regions. The decline of and unsustainable hunting (Kamp et al., 2015). Meanwhile,
many species has been linked to anthropogenic changes in habitat the lack of understanding of regional population trends and
conditions, such as habitat loss and fragmentation (Robinson status of many East and Southeast Asian species continues
and Wilcove, 1994) intensified by climate change (Lloyd-Evans to hamper conservation actions targeting landbird species.
and Atwood, 2004; Sanderson et al., 2006; Vickery et al., 2014; They are similarly affected by inconsistent and incomplete
Gilroy et al., 2016). Over time, climate change is expected to levels of protection offered by national and international legal
disrupt ecological and environmental processes that may affect frameworks for wildlife conservation (Runge et al., 2015;
migration and reproduction, for instance, by driving spatio- Yong et al., 2015, 2018).
temporal mismatches in food resources (Carey, 2009). Given Since 2010, growing interest in the ecology and conservation
that migratory species have geographically complex life cycles of migratory landbirds in the EAF has yielded fresh insights on
that connect breeding, stopover and non-breeding sites over their migration ecology and migratory connectivity (Yamaura
large areas, they are especially vulnerable to threats along their et al., 2017; Heim et al., 2018b, 2020; Choi et al., 2020b; Uemura
et al., 2020), species-specific population declines (Tamada et al.,
migratory routes (Runge et al., 2014, 2015).
2014, 2017; Kamp et al., 2015; Edenius et al., 2017; Choi
The East Asian Flyway (EAF) as defined here overlaps with
et al., 2020a), and threats (Amano and Yamaura, 2007; Iqbal
the eastern hemisphere (east of the 90th meridian), including
et al., 2014; Kamp et al., 2015). While large-bodied hawks and
the western Pacific Ocean (McClure, 1974, 1984; Nisbet, 1976;
eagles (Accipitriformes) have traditionally been easier to study
Yong et al., 2015), and spans arctic, boreal, temperate and tropical during migration (Higuchi et al., 2005; Reading et al., 2020)
biomes (Figure 1). Compared to the African-Eurasian and the and at key bottleneck sites (Zalles and Bildstein, 2000; Yamazaki
American flyways, the EAF is geographically more varied with et al., 2012; DeCandido et al., 2015; Limparungpatthanakij
an uneven distribution of landmass across boreal-temperate and et al., 2019), studies on migratory passerines and other
tropical latitudes (Nisbet, 1976). While there are few ecological landbirds are fast catching up thanks to emerging tracking
barriers in the west in the form of mountain ranges, the EAF technology and methods.
contains extensive island chains at its eastern fringe and the vast Against this ‘migratory landbird renaissance,’ we aim to
Indo-Australian archipelago spanning the tropical belt. These synthesize existing knowledge on the conservation status of
island chains collectively pose complex barriers in the form of migratory landbirds (see Table 1 for definitions) in the EAF.
sea-crossings for migrating landbirds (Kuroda, 1961; Ellis et al., We also identify key knowledge gaps for further work in
1990; Yamazaki et al., 2012; Nourani et al., 2018) unmatched this traditionally data-poor migratory flyway. We define the
in other flyways. taxonomic scope of landbirds in our review based on the
With almost 400 species (387 species [63% of all migratory widely accepted definitions used in the literature (Kirby et al.,
species]; see also Appendix I for full list), the bulk of EAF 2008; Faaborg et al., 2010), which encompasses passerines,
migratory species are in fact landbirds, with passerines and raptors and several near-passerine families (see Supplementary
diurnal raptors among the most species-rich groups (McClure, Data for full taxonomic scope). We (1) summarize recent
1974; Yamazaki et al., 2012; Yong et al., 2015). In this flyway, advances in landbird migration ecology research in the EAF,
migratory landbirds fulfill diverse ecological roles in boreal, (2) review emerging evidence of declines and associated drivers
temperate and tropical biomes in terms of their trophic positions in key biomes, (3) discuss the ecological implications of these
(e.g., herbivory, insectivory and predation) and transport changes on Asian ecosystems in the wider context of land use
processes (e.g., nutrient and parasite transfer, seed and pollen change and unsustainable hunting, and (4) identify knowledge
dispersal; see Şekercioğlu et al., 2004; Bauer and Hoye, 2014; gaps and describe how addressing them can translate into
López-Hoffman et al., 2017). Across East Asia, migratory conservation actions.
landbirds consume and disperse the fruits and seeds of varied tree
species, as evidenced by studies in Japan, China and South Korea
(Nakanishi, 1996; Corlett, 1998; Choi and Chae, 2007; Cho et al., ADVANCES IN LANDBIRD MIGRATION
2011; Choi et al., 2011; Jeong et al., 2014). Insectivorous species ECOLOGY IN THE EAF
provide significant pest-control services to agroecosystems (Kim
et al., 2012b) and directly reduce disease transmission through Understanding the different migration strategies used by
predation and scavenging (Kim et al., 2012a). Yet, despite their landbirds is crucial to conservation at sites used over the annual
contribution to ecosystems at a large scale in East and Southeast cycle of migratory birds. Building on long-term bird ringing work
Asia, landbirds are the least understood among the diverse in Japan, the Russian Far East, China and South Korea (reviewed
migratory bird assemblages in Asia (Yong et al., 2015; Heim et al., in McClure, 1974; Yong et al., 2015), several new large-scale
2020).
ringing projects have been established in this region, for instance
The declines in populations of many migratory waterbirds,
in India and Mongolia (Buner et al., 2015; Davaasuren, 2018).
and especially shorebirds, across East Asia and Australasia
have been well documented (Szabo et al., 2016; Studds et al.,
2017) and are far better understood than landbird declines. Research on Migration Strategies and
However, Emberiza buntings and many other East Asian Stopover Ecology
landbirds have suffered dramatic population declines in recent In general, the migration strategy of a species is fundamentally
years (Kamp et al., 2015; Edenius et al., 2017; Choi et al., 2020a), shaped by its habitat requirements and physiology. Many species
driven in part by habitat loss (Higuchi and Morishita, 1999) that cover long distances need to refuel several times to replenish
Frontiers in Ecology and Evolution | www.frontiersin.org 2 April 2021 | Volume 9 | Article 613172
Yong et al. Conservation of East Asian Landbirds FIGURE 1 | The extent of the East Asian Flyway (EAF) bounded by the 90th meridian on the west and the Pacific Ocean on the east including boreal, temperate and tropical biomes. Data from The Nature Conservancy. Terrestrial ecoregions (2020). https://tnc.maps.arcgis.com/home/item.html?id=7b7fb9d945544d41b3e7a914 94c42930 (accessed May 10, 2020). Frontiers in Ecology and Evolution | www.frontiersin.org 3 April 2021 | Volume 9 | Article 613172
Yong et al. Conservation of East Asian Landbirds
TABLE 1 | Definitions of key terms mentioned in the text.
Term Definition Example
Altitudinal migrant Species that breed at higher altitudes and migrate across elevational gradient over scarlet finch Haematospiza sipahi, collared
seasons. Some species may also cross latitudinal gradients. grosbeak Mycerobas affinis, various genera in
Leiothrichidae
Biome Distinct (broad) communities of plants and animals that have formed in response to a
shared climate.
East Asian Flyway A broad network of migratory routes used by populations of landbird species that
connect the northern and eastern Asian breeding areas with non-breeding areas at
lower latitudes, especially in tropical Asia and extending to insular Southeast Asia. Also
referred to as the East Asian-Australasian Flyway when used in the context of the many
shorebirds species that migrate to overwinter in Australasia.
Intra-tropical migrant Migratory species that breed, migrate and winter largely within the tropical/subtropical blue-winged pitta Pitta moluccensis, Asian
latitudinal belt. emerald cuckoo Chrysococcyx maculatus,
Asian drongo cuckoo Surniculus lugubris
Long-distance migrant Species that migrate large distances (c. 2,000–10,000 km) at a continental scale common stonechat Saxicola torquatus,
annually, typically covering several biomes and a wide range of latitudes. These species Japanese sparrowhawk Accipiter gularis,
usually lack sedentary populations. oriental cuckoo Cuculus optatus
Migratory corridor A series of migratory routes used by multiple species, defined by particular geography
of the region (See Figure 2).
Migratory connectivity Linkages between migratory populations of a species at the breeding and non-breeding
areas, including stopover sites.
Short-distance migrants Species that migrate relatively short distances (
Yong et al. Conservation of East Asian Landbirds
FIGURE 2 | Autumn migration routes of landbirds in the EAF, including one individual track for each all species for which published data is available (n = 21).
(A) Non-passerines (illustration of Oriental honey buzzard Pernis ptilorhynchus), (B) Passerines (illustration of Siberian rubythroat Calliope calliope). Based on Ueta
et al. (1998, 2000), Higuchi et al. (2005), Shiu et al. (2006), Kim et al. (2007), Kudo (2008), McIntyre et al. (2009), Dixon et al. (2011, 2012), Kessler et al. (2013),
Takagi et al. (2014), Koike et al. (2016), Yamaura et al. (2017), Yamaguchi et al. (2017), Heim et al. (2018a, 2020), Choi et al. (2019), and Uemura et al. (2020). Bird
illustrations reproduced with permission of Lynx Edicions/Handbook of the Birds of the World.
autumn, and of these, species breeding at higher latitudes tend species and populations (Finch et al., 2015; Heim et al., 2020;
to pass earlier during spring migration (Wobker et al., 2021). Figure 2A). As smaller devices become increasingly available,
Additionally, biological factors, such as sex, age and the timing various small-bodied landbirds can now be effectively tracked.
of molt are all known to influence migration phenology in many Over the past decade, the number of landbird species tracked in
passerines (Maslovsky et al., 2018; Park et al., 2020; Wobker et al., the EAF has steadily risen to at least 26 species, with an increasing
2021), with protandry being a common pattern (Nam et al., 2011; number of small passerines (Figures 2A,B and Table 2).
Bozó and Heim, 2016; Park et al., 2020). Two main migratory corridors in the EAF are now well
Monitoring migration phenology is important, given that the established, (1) the ‘island’ or ‘oceanic’ route linking eastern
ability of a species to adjust its migration timing to events along Russia (Kamchatka and Sakhalin) and Japan to the Philippines
its annual cycle can indicate its vulnerability to climate change and eastern Indonesia, and (2) the ‘mainland’ route, linking
(Møller et al., 2008). Valchuk et al. (2017) suggested that links eastern Russia, China and continental Southeast Asia (Higuchi,
between the West Pacific climate index and the abundance of 2005; Yamazaki et al., 2012; Concepcion et al., 2017; Heim et al.,
migrating landbirds at a stopover site in the Russian Far East can 2020). Data from recent tracking studies (Figure 2) further
indicate the effects of climatic shifts on migration phenology at illustrate the use of the ‘island route’ by passerines and raptors
a broad scale. Indeed, long-term studies have revealed shifts in breeding in Japan (Koike et al., 2016; Nourani et al., 2018;
spring arrival times for several species in Japan, linked to warmer Uemura et al., 2020) and species shared with Kamchatka (e.g.,
temperatures (Deguchi et al., 2015), consistent with observations barn swallow Hirundo rustica and Siberian rubythroat) (Heim
in Europe and the Americas (Thorup et al., 2007; Hurlbert and et al., 2020). These results corroborate direct observations in
Liang, 2012). the Philippines and eastern Indonesia (Germi et al., 2009, 2013;
Concepcion et al., 2017).
Research on Migratory Routes and The specific island route(s) used remain poorly studied.
Connectivity Observational data show that two raptors, grey-faced buzzard
Studying the migratory connectivity of a species is necessary Butastur indicus and Chinese sparrowhawk Accipiter soloensis,
to understand its migration ecology (Marra et al., 2011), pass south through the Japanese archipelago, Taiwan and the
and holds important implications for its conservation. Data Philippines (Ellis et al., 1990; Yamazaki et al., 2012; Concepcion
from ringing recoveries, increasingly complemented with data et al., 2017). Similarly, some passerines, including wagtails, pipits
obtained from various tracking technologies (e.g., light-level and yellow bunting Emberiza sulphurata, also follow this least
geolocators and satellite telemetry) have traditionally been used energetically costly route (Nourani et al., 2018). Certain species
to map migration routes, and infer migratory connectivity for may take a more direct route from south Japan passing east
Frontiers in Ecology and Evolution | www.frontiersin.org 5 April 2021 | Volume 9 | Article 613172
Yong et al. Conservation of East Asian Landbirds
TABLE 2 | East Asian landbird migrants for which tracking data have been published in the peer-reviewed literature (n = 23) with the tracking technique (Tech) used for
each species (GLS = light-level geolocation, GPS = Global Positioning System data logging and SAT = satellite tracking), the number of individuals tracked (N,
adults/juveniles), the country where the birds were tagged (RUS = Russia, MNG = Mongolia, JPN = Japan, USA = United States of America), and the source(s) where the
original data were published.
Species Tech N Country Source
Cuckoos
Common cuckoo1 SAT 4/0 RUS Bulyuk et al., 2018; Thorup et al., 2020
Bustards
Great bustard SAT 3/0 MNG Kessler et al., 2013
Raptors
Oriental honey buzzard SAT >33/1 JPN Higuchi et al., 2005; Shiu et al., 2006; Yamaguchi et al., 2008,
Yamaguchi et al., 2012; Sugasawa and Higuchi, 2019
Cinereous vulture GPS/PTT 10/53 KOR/MNG Kim et al., 2007; Reading et al., 2020
Northern goshawk SAT 2/0 JPN Kudo, 2008
White-tailed sea eagle SAT 2/0 JPN Ueta et al., 1998
Steller’s sea eagle SAT 9/25 JPN/RUS Meyburg and Lobkov, 1994; Ueta et al., 2000; McGrady et al., 2003
Grey-faced buzzard SAT 9/0 JPN Shiu et al., 2006; Nourani et al., 2018
Rough-legged buzzard SAT 4/0 JPN Yamaguchi et al., 2017
Pigeons
Japanese wood pigeon GPS 23 KOR Choi et al., 2019
Kingfishers
Ruddy kingfisher GPS 3/0 JPN Uemura et al., 2020
Falcons
Amur falcon1 SAT 1/0 MNG Dixon et al., 2011
Gyrfalcon SAT 0/154 USA McIntyre et al., 2009
Peregrine falcon SAT 17/0 RUS Dixon et al., 2012
Passerines
Black-naped oriole GLS 1/0 RUS Heim et al., 2020
Brown shrike GLS 3/0 JPN Aoki et al., 2020
Rook SAT 20/0 JPN Takagi et al., 2014
Pallas’s grasshopper warbler GLS 1/0 RUS Heim et al., 2020
Red-rumped swallow GLS 1/0 RUS Heim et al., 2020
Barn swallow GLS 1/0 RUS Heim et al., 2020
Willow warbler2 GLS 3/0 RUS Sokolovskis et al., 2018
Chestnut-cheeked starling GLS 16/0 JPN Koike et al., 2016
Chinese blackbird SAT 0/1 KOR Choi et al., 2020c
Siberian rubythroat GLS 10/0 RUS Heim et al., 2018b, 2020
Common stonechat GLS 12/0 JPN Yamaura et al., 2017
Yellow-breasted bunting GLS 3/0 RUS Heim et al., 2020
Note that the migration routes of some species extend beyond the East Asian Flyway1,2 . 1 Migrates to Africa via India; 2 migrates to Africa via West Asia; 3 ages unknown;
4 only four individuals migrated from Alaska to East Asia.
of Taiwan, most likely aided by seasonal weather conditions, rubythroat, Pallas’s grasshopper warbler Locustella certhiola and
as suggested by tracking data of ruddy kingfisher Halcyon yellow-breasted bunting Emberiza aureola) (Heim et al., 2018b,
coromanda, chestnut-cheeked starlings Agropsar philippensis and 2020), as well as for great bustard (Kessler et al., 2013) and
grey-faced buzzards (Koike et al., 2016; Uemura et al., 2020). cinereous vulture Aegypius monachus (Kim et al., 2007; Reading
The northward migration route(s) in spring is less well known, et al., 2020). Although there are no major geographical barriers,
with some species supposedly leaving the northern Philippines species using the ‘mainland route’ may cross uplands and
heading for southern China (Welch, 2011). The low number mountains in central and southern China, northern Indochina
of observations of species such as Gray’s grasshopper warbler (Wang et al., 2000; Tordoff, 2002; Fei et al., 2015) and the Malay
Locustella fasciolatus in Taiwan and the Philippines is unusual Peninsula (Medway and Wells, 1976).
(Severinghaus et al., 2017; Allen, 2020) – either they largely Based on satellite tracking studies, Oriental honey buzzards
overfly or bypass these islands, or are simply overlooked. breeding in Japan (Higuchi et al., 2005; Yamaguchi et al.,
Meanwhile, recent tracking data from Russia, Mongolia and 2008, 2012; Sugasawa and Higuchi, 2019) and probably yellow-
northern China are providing insights on precise migration paths breasted buntings from Kamchatka (Heim et al., 2020) make
along the ‘mainland route’ for small passerines (e.g., Siberian major sea crossings to the mainland before migrating to
Frontiers in Ecology and Evolution | www.frontiersin.org 6 April 2021 | Volume 9 | Article 613172Yong et al. Conservation of East Asian Landbirds
southern China and Southeast Asia (Yamaura et al., 2017), 1966; Won and Gore, 1971), whilst natural history studies of
potentially avoiding longer sea crossings further south. Such many species exist.
migratory patterns may suggest that these species colonized The broad distribution of birds in the eastern Palearctic
Japan from the mainland relatively recently (Agostini and (which overlaps in its entirety with the northern EAF) was
Mellone, 2007). Satellite telemetry has demonstrated strong first described by Shtegman (1938), who defined seven major
migratory linkages for large (soaring) species, particularly rough- habitat-associated groups across the wider Palearctic region.
legged buzzards Buteo lagopus moving between eastern Russia Based on this classification, most migratory landbird species
and Japan (Yamaguchi et al., 2017), while highlighting the in the EAF (finches, chats, thrushes, buntings and Phylloscopus
importance of Japan for wintering Steller’s sea eagles Haliaeetus warblers) belong to the Siberian (usually boreal forest or
pelagicus and white-tailed sea eagles H. albicilla breeding in taiga species) or the Chinese faunal group (usually species
eastern Russia (Ueta et al., 1998; McGrady et al., 2003). of mixed broadleaf forests; see Shtegman, 1938). The ratio
Similarly, tracking studies and field observations at key watch of migratory species progressively increases with latitude: the
sites have demonstrated the role of the Japanese archipelago handful of Arctic-breeding species are almost all migratory,
as a land corridor for bird migration into tropical Asia while the proportion of migratory species drops to 60–80% in
(Shiu et al., 2006; Yamazaki et al., 2012; Koike et al., 2016; the boreal and temperate biomes (Ganter and Gaston, 2013;
Nourani et al., 2018). Somveille et al., 2013), and even lower in the subtropics
Nevertheless, whilst the majority of EAF landbird species (Yong et al., 2015).
migrate largely along latitudinal gradients into temperate and
tropical Asia, a few species deviate from these two major
migratory corridors to reach non-breeding grounds in India DISTRIBUTION AND ECOLOGY OF
or Africa. These landbirds have migratory routes that partially MIGRATORY LANDBIRDS IN THE TROPICS
overlap with the EAF; they eventually migrate westward toward
Africa crossing the large ecological barrier of the Indian Ocean. The broad patterns associated with wintering landbird diversity
Two of the best studied examples are Amur falcon Falco and distributions across tropical Asia are relatively well described
amurensis and common cuckoo Cuculus canorus, both known to (Nisbet, 1976; White and Bruce, 1986). The diversity of wintering
cover the longest migratory distances among East Asian landbirds landbirds is highest in mainland Southeast Asia, followed by
(Dixon et al., 2011; Townshend, 2016a; Bulyuk et al., 2018; southern China and the Greater Sundas (McClure, 1974; Nisbet,
Figure 2A). 1976; Yong et al., 2015; Table 3), declining progressively through
the Philippines and Wallacea toward Australia (White and Bruce,
1986). Unlike other Eurasian migratory systems, the EAF hosts a
BREEDING DISTRIBUTION OF large number of insectivorous species that overwinter in forests,
MIGRATORY LANDBIRDS many with putative and/or narrow distributions (e.g., rufous-
headed robin, blackthroat Calliope obscura, Gansu leaf-warbler
The varied ecosystems of northeast Asia form the core breeding Phylloscopus kansuensis and Ijima’s leaf-warbler Phylloscopus
grounds of most migratory landbirds in the EAF (McClure, ijimae; see Yong et al., 2015). A few species, such as Gray’s
1974; Nisbet, 1976; Yong et al., 2015). These include temperate grasshopper warbler Locustella fasciolata may be considered
broadleaf forests in China, Japan and the Korean Peninsula, ‘extreme eastern’ landbird migrants that largely overwinter in
which support the highest diversity of (migratory) breeding eastern Indonesia (White and Bruce, 1986; Coates and Bishop,
landbirds, as well as boreal (taiga) forests and Arctic tundra, 1997; Allen, 2020). A handful of taxa have their core wintering
which support a more depauperate breeding landbird fauna ranges in New Guinea or continental Australia (e.g., white-
(Ganter and Gaston, 2013; Figure 3). There are fewer than 20 throated needletail Hirundapus caudacutus) (White and Bruce,
landbird species regularly breeding in the Arctic, only five of 1986; Tarburton, 2014; Menkhorst et al., 2017).
which are strictly associated with this biome (Vaughan, 2010; Tropical broadleaf forests form the dominant wintering
Ganter and Gaston, 2013). The migration patterns of Arctic- habitat for at least 90 migratory landbirds in the Southeast Asian
breeding landbirds are not well known, as the movements tropics (Medway and Wells, 1976; Wells, 2007; Yong et al., 2015;
of only one species, the snow bunting Plectrophenax nivalis, Figure 4). An additional 60 species that rely on this habitat are
have been tracked and only in an American flyway (McKinnon Sino-Himalayan and/or short-distance migrants that breed at
et al., 2016). The natural history of the landbirds of eastern higher (subtropical and tropical) latitudes. The ecological niches
Russia, which forms the largest part of the EAF, has, however, occupied by these forest-dependent species vary considerably.
been relatively well studied for over a century (Dementiev Many occupy seasonal deciduous and evergreen forest mosaics,
and Gladkov, 1951–1954). Extensive regional reviews are also species wintering in the Greater Sundas mostly use evergreen
available for northeast Russia (Kistchinski, 1968, 1988; Krechmar (lowland) rainforests, while the few species reaching southern
et al., 1991), Sakhalin Island (Nechaev, 1991) and the diverse Wallacea are largely eurytopic (Schellekens et al., 2011). The
broadleaf temperate forest of Primorsky Krai (Gluschenko elevational distribution of most forest-wintering taxa has been
et al., 2016). Similarly, reviews have been published on the poorly defined, although some seem to be confined to lowlands
Chinese, Korean and Japanese breeding bird fauna since the or mountains (15 and 23 species, respectively). At least
1960s (Cheng and Li, 1955; Yamashina, 1961; Won et al., 36 species use inland freshwater wetlands, opportunistically
Frontiers in Ecology and Evolution | www.frontiersin.org 7 April 2021 | Volume 9 | Article 613172Yong et al. Conservation of East Asian Landbirds FIGURE 3 | Six major biomes in northeast Asia form the breeding range of most migratory landbirds in the EAF (Image credits: Pavel Ktitorov, Tiah Khee Lee, Heng Yee Cheng, Yann Muzika, Bjorn Olesen, Geoff Lim). exploiting wetland-like rice paddies (Figure 4) that represent the their distribution to colonize new habitats created by the dominant anthropogenic land cover in many parts of tropical clearance of the climax vegetation (Yamaura et al., 2017). Asia (Round, 2008). As the region was formerly dominated In Indonesia, starlings and other wintering species are now by forests, the historical distribution of species assemblages reported from urban areas and heavily modified mosaics of currently associated with open anthropogenic landscapes is coastal vegetation (Diniarsih et al., 2016), suggesting some level unclear. Nevertheless, some almost certainly have expanded of adaptability. Frontiers in Ecology and Evolution | www.frontiersin.org 8 April 2021 | Volume 9 | Article 613172
Yong et al. Conservation of East Asian Landbirds
TABLE 3 | Non-breeding distribution of migratory landbirds in different Southeast Asian regions and Australia.
Region Number of species (exclusive) Shared with Number of species
Australia 1 Philippines 1
Philippines 13 Greater Sundas and Thai-Malay Peninsula 16
Greater Sundas and Thai-Malay Peninsula 14 Philippines, Indochinese Peninsula* 9
Indochinese Peninsula* 124 Greater Sundas and Thai-Malay Peninsula 23
Wide-ranging species 29
*Includes species in adjacent southern China (e.g., Yunnan and Hainan).
POPULATION TRENDS OF LANDBIRDS buntings Emberiza rutila, were found to have declined in
IN EAST ASIA – THE CURRENT EVIDENCE South Korea (Choi et al., 2020a). In Russia, significant declines
have been detected for Pallas’s E. pallasi (Heim, 2017) and
Ever since Silent Spring (Carlson, 1962) raised the alarm on bird chestnut bunting (Valchuk et al., 2017) on migration and at
declines globally, landbird population declines have been widely breeding sites (Ananin, 2011). These patterns are consistent with
reported in Europe and North America (Terborgh, 1992; Vickery the declining trends of passerine landbirds reported at ringing
et al., 2014; Rosenberg et al., 2019). Long-term population stations in mainland China (Jiao et al., 2016; Xu et al., 2017)
trends for European species became available based on the large and at breeding sites surveyed in Japan and Taiwan (Tamada
datasets collected by various large-scale bird monitoring and et al., 2014, 2017; Kitazawa et al., 2020; Japan Bird Research
ringing schemes (Vorisek et al., 2008). In East Asia, the first Association, 2021), including the threatened fairy pitta Pitta
worrying trends were detected in Japan, with declines found to nympha (Lin and Pursner, 2020). Meanwhile, population trends
be associated with forest-dependent and long-distance migrant of landbirds on their wintering grounds remain largely unknown,
species (Higuchi and Morishita, 1999; Amano and Yamaura, even though the available evidence suggests declines for species
2007), and further evidenced in Japan’s national-level bird atlas that winter in India (SoIB, 2020) and Australia (Tarburton, 2014;
(Japan Bird Research Association, 2021). Wells (2007) reported see also Supplementary Table 1).
larger declines for landbirds that rely on tropical forests as While many long-distance Asian migrants including those
wintering habitat in the Thai-Malay Peninsula and data from wintering in the tropics have suffered larger declines (Amano
Thailand also suggest a decline of at least some species (e.g., tiger and Yamaura, 2007; Bourski, 2009; Ananin, 2011), consistent
shrike Lanius tigrinus; Round, 2010). with patterns observed in the Western Palearctic (Vickery et al.,
In the past decade, drastic declines in the yellow-breasted 2014), the trends are inconsistent, even among species that
bunting (Figure 5) have raised major conservation concerns share apparently similar migration strategies. The yellow-browed
(Kamp et al., 2015). This species used to be one of the most warbler has declined at both its breeding and wintering grounds
abundant Palaearctic birds with a vast breeding distribution (Ananin, 2010, 2011; Xu et al., 2017; SoIB, 2020), while increases
from Fennoscandia to eastern Russia and Japan (Dementiev and have been documented for the closely related dusky warbler
Gladkov, 1951–1954; McClure, 1974). However, since the 1990s, Phylloscopus fuscatus (Ananin, 2011; Gerasimov and Lobkov,
its global population has declined by almost 90% (Kamp et al., 2019). There is an urgent need to understand overall population
2015), with national-level declines reported from Russia, Japan trends for migratory landbird species, drawing from monitoring
and Korea (Tamada et al., 2014, 2017; Choi et al., 2020a; Park work across the region. This will also help elucidate the specific
et al., 2020; Heim et al., in press) and the species was uplisted threats and drivers of decline.
to Critically Endangered in 2017 (BirdLife International, 2020).
A similar trend has been documented for the closely related
rustic bunting Emberiza rustica, based on data from the breeding RANGE SHIFTS OF LANDBIRDS
grounds in Russia (Yakovleva and Sukhov, 2017; Gerasimov
and Lobkov, 2019), Fennoscandia and from stopover sites in Some observed changes in species population trends and
China and Japan (Edenius et al., 2017). Buntings are typically densities of landbirds can be explained by shifts in breeding
widely distributed and thus data on their status and trends are distributions and range limits. Many European and North
available from multiple sites across their breeding range. Yet, for American species show recent range shifts likely driven by
the majority of East Asian species with narrower distributions, changes in habitat availability accelerated by climate change
little or no long-term monitoring data are available and it is (Virkkala and Lehikoinen, 2014; Whitaker, 2017). Similarly, in
nearly impossible to confidently elucidate population trends or the EAF, northward and eastward shifts have been detected in the
conservation status (Yong et al., 2015). breeding distribution and range limits of several species across
Across the region, evidence for the decline of migratory eastern Asia. Some Chinese breeding species (e.g., red-billed
landbirds has been growing steadily based on studies at stopover starling Sturnus sericeus, light-vented bulbul Pycnonotus sinensis
sites and the breeding grounds (see Supplementary Table 1). and yellow-bellied tit Parus venustulus) were not recorded in the
Based on diverse data sources, six breeding and migrating Korean Peninsula until 2000. All three have since expanded their
bunting species, including the once abundant rustic and chestnut distribution ranges northeast across the Yellow Sea and became
Frontiers in Ecology and Evolution | www.frontiersin.org 9 April 2021 | Volume 9 | Article 613172Yong et al. Conservation of East Asian Landbirds FIGURE 4 | Relative importance of biomes in tropical Asia for wintering migratory landbirds. Cultivated land, such as rice paddies, is among the most important of the human-modified landscapes for migratory landbirds (Image credits: Yong Ding Li). Grey bars (breeding species), white bars (wintering species), black bars (species on stopover). locally common breeding species in South Korea (Choi et al., records east of the Verkhoyansky Mountains. Since 2009, the 2011). The range of the yellow-bellied tit has expanded even species has rapidly spread eastward, reaching Magadan in 2014 further north and it has colonized the Russian Far East (Fetting (Kondratyev, 2014), Kamchatka (Lobkov, 2015) and the Anadyr et al., 2016; Redkin et al., 2020). The widespread Palearctic- River by 2020, a range extension of more than 1,000 km. breeding fieldfare Turdus pilaris has shown a recent eastward There are other examples of range shifts at smaller spatial expansion across Siberia. At the end of the 20th century, fieldfares scales, as well as longitudinal shifts along the tundra-forest- bred as far east as Yakutia, west of the Aldan River, with no tundra gradient, and in the northern taiga transition zones. Little Frontiers in Ecology and Evolution | www.frontiersin.org 10 April 2021 | Volume 9 | Article 613172
Yong et al. Conservation of East Asian Landbirds
colonized the northern parts of the island. In temperate and
subtropical areas of China, several migratory cuckoo species have
exhibited northward and eastward shifts (Sun et al., 2018).
Shifts in distributions and range limits of many species may
be explained by changes in vegetation cover and associated
habitat dynamics, often anthropogenically caused, or may arise
due to the broader effects of warming driven by climate change
(Virkkala and Lehikoinen, 2014; Box 1). According to modeled
climate change scenarios, the distributions of most East Asian
species are expected to be affected, including many that are
already threatened (Hu et al., 2020). These distribution shifts
need to be considered when planning conservation actions for
migratory species. While there is a risk that observed distribution
shifts may arise from geographical biases in sampling, they need
to be monitored and carefully documented, as they may manifest
in precipitous local declines, as seen in the near-endemic Japanese
breeding subspecies of brown shrike (Kitazawa et al., 2020).
FIGURE 5 | Yellow-breasted bunting Emberiza aureola is the best example of
an Asian landbird that has suffered steep declines in the recent decade (Kamp
et al., 2015; Image credits: Michelle and Peter Wong).
THREATS TO MIGRATORY LANDBIRDS
The threats faced by migratory landbirds in the EAF are poorly
understood compared with those faced by waterbirds, which
bunting Emberiza pusilla, Arctic warbler Phylloscopus borealis have been extensively studied in the past decade (Studds et al.,
and Common stonechat Saxicola torquatus, all characteristic 2017; Gallo-Cajiao et al., 2020). Given that most landbirds in
boreal species, have shifted northwards and breed more regularly the region (Figure 4) are somewhat dependent on forests as
in the tundra and at more diverse locations than previously stopover and non-breeding habitat, forest loss and degradation
known (Andreev et al., 2015; Syroechkovskiy et al., 2019). are predicted to be major threats. Intensive land management,
On Sakhalin Island, black-browed reed warbler Acrocephalus especially intensive agriculture, often with heavy pesticide use,
bistrigiceps (Ktitorov and Zdorikov, unpublished data), and presumably also affects species stopping over or wintering in rice
White’s thrush Zoothera aurea (Ktitorov et al., 2019) have recently paddies or other cultivated land. It remains unclear how complex
BOX 1 | Land cover change in eastern Siberia and the Russian Far East: impacts on breeding birds.
The varied and complex ecosystems of eastern Siberia and the Russian Far East provide breeding grounds for most long-distance migratory landbirds in the EAF
(Figure 3). Much of eastern Russia has a sparse human population and thus appears little disturbed, based on the limited extent of built environments, population
density and infrastructure (Venter et al., 2016). Not surprisingly, this understudied, but ecologically complex region is frequently perceived as being covered by vast
tracts of boreal forests. However, recent global assessments of intact forested landscapes reveal that the extent of old-growth forest cover is less than expected and
is declining even in the most remote areas of eastern Russia (Potapov et al., 2008, Potapov et al., 2017; Global Forest Watch, 2014).
The main drivers of deforestation and land use change in eastern Russia include legal and illegal logging, both which are unsustainable (Vandergert and Newell,
2003), and fire. While most forest fires (65%) are anthropogenic, their prevalence has increased as a result of the earlier spring and summer thaw, presumably
exacerbated by climate change (Achard et al., 2008). Logging and forest fires mostly affect the more developed, southern regions of the Russian Far East (Kurdykov
and Volkovskaya-Kurdyukova, 2016; Heim et al., 2019), but forest fire hotspots are becoming increasingly prevalent further north, particularly in central Yakutia and
have even penetrated the forest-tundra zone of southern Chukotka (Achard et al., 2006).
Land cover changes associated with shifting agricultural policies have attracted less attention, but have a discernible effect in shaping Siberian ecosystems. The
collapse of the Soviet Union in 1991 triggered the abandonment of vast areas of cropland and pasture, especially in southern Siberia and in the Far East. Since
2016, some areas have reverted to agriculture (Prishchepov et al., 2020), but these remain negligible in eastern Russia, mostly concentrated along the Chinese
border (Teluguntla et al., 2015: Global Cropland Database). This synergy of anthropogenic drivers and natural ecological processes is re-shaping landscapes in
eastern Russia and has resulted in the replacement of the mosaic of old-growth forests and cultivated land by more uniform early- and mid-successional shrub or
forest habitat (Heim et al., 2019), although some areas of old-growth forest show signs of recovery (Potapov et al., 2008, Potapov et al., 2017).
In the Arctic and sub-Arctic regions of eastern Russia, changes in the vegetation cover, particularly in the tundra and taiga-tundra ecotone have received little
attention from ecologists. One of the most visible features of the Arctic landscape associated with climate change is ‘shrubification,’ characterized by an increase in
cover, height and thickness of shrub vegetation (Tape et al., 2006; Forbes et al., 2010). In the eastern Russian tundra, larch Larix spp. and willow Salix spp. are
growing taller, leading to gradual transformation of the taiga-tundra transition zone into true taiga and the encroachment of shrubland into tundra (Forbes et al.,
2010; Frost and Epstein, 2014; Heim et al., 2021). Remote sensing analyses show hotspots of tundra greening in many areas of the Russian Arctic
(Frost and Epstein, 2014).
The large-scale consequences of land cover change for migratory landbirds have not been studied, partly due to the lack of a nation-wide bird monitoring
scheme in Russia. However, these changes are presumably complex and multi-directional, affecting species dependent on old-growth forests negatively, but
favoring species that exploit post-fire successional vegetation and forest edges (Osipov and Biserov, 2017). Based on the observed directionality of vegetation
change, it is possible to make some broad predictions: (1) forest edge and shrub-dwelling species (i.e., most boreal-breeding migratory passerines) should benefit
from increased habitat availability, while (2) old-growth forest species (e.g., large diurnal and nocturnal raptors) and (3) open habitat species (e.g., various bunting
species) may suffer from a reduction of habitat.
Frontiers in Ecology and Evolution | www.frontiersin.org 11 April 2021 | Volume 9 | Article 613172Yong et al. Conservation of East Asian Landbirds
land use changes and land management regimes will impact bird harvest period coincides with the arrival of migratory species.
populations across Asia under different climate change scenarios. The leftover stubble is used by raptors, insectivores, such as
Meanwhile, the intense harvesting of wildlife for use as food bluethroat Luscinia svecica and eastern yellow wagtail Motacilla
or pets has been directly implicated in the decline of several tschutschensis, and granivores, such as yellow-breasted bunting
migratory landbirds in the EAF, the best known being the yellow- (McClure, 1974; Round, 2008). Similar examples have been
breasted bunting Emberiza aureola (Chan, 2004). documented in Indochina, Malaysia and southern China (Wong
et al., 2009; Azman et al., 2019). In Timor in Wallacea, heavily
Habitat Loss and Degradation grazed and modified floodplains support a few migratory species,
Forest loss and degradation affect many migratory landbirds such as eastern yellow wagtail (Trainor et al., 2007).
throughout their distributions in the EAF, particularly at the Widespread land-use change, in particular agricultural
tropical wintering grounds (Amano and Yamaura, 2007; Yong intensification with the associated loss of fallow and increased
et al., 2015). Asian tropical lowlands have suffered the highest pesticide use, may have contributed to the declines of wintering
rates of forest loss globally (Corlett, 2014; Stibig et al., 2014; buntings in Southeast Asia, and species that feed on large insects,
Namkhan et al., 2021). Extensive deforestation throughout the such as shrikes and drongos (Round, 2008; Kitazawa et al., 2019).
lowlands of the Greater Sundas is predicted to affect both globally Meanwhile, changing water management and cropping regimes
threatened and more common species that winter predominantly in rice paddies may affect wintering landbird assemblages to the
in lowland forest (Wells, 2007; Yong and Liu, 2015). In one detriment of species with specialised ecological needs. Across
of few assessments of wintering forest landbird assemblages, Southeast Asia, formerly rain-fed, single-crop rice (including
Wells (2007) observed that the densities of Siberian blue robin floating rice) has now been extensively replaced by multi-
Larvivora cyane were substantially lower in Malaysian hill-slope cropped rice that demands intensive irrigation (Round, 2008).
forests and in disturbed or agricultural habitats compared to An associated reduction in fallow duration and the extent of
old-growth lowland rainforests, suggesting that this common fallow fields and paddy stubble may reduce food resources and
wintering species is sensitive to lowland deforestation. habitat available to wintering birds. In the floodplain wetlands of
Montane forest cover in Southeast Asia has been relatively less Candaba in Luzon (the Philippines), which was the only known
affected compared to the lowlands (Soh et al., 2019), and therefore regular wintering site for the Endangered streaked reed-warbler
species wintering in montane forests have been presumed to Acrocephalus sorghophilus, the original natural wetlands have
face lower risk. Yet, montane forests are also under increasing been converted to rice paddies, while intensive land management
pressure (Peh et al., 2011; Zeng et al., 2018). In northeast practices limit natural succession, reducing possibly essential
India and Bangladesh, deforestation on mountains is driven habitat diversity (Round and Allen, 2010).
by illegal logging and clearing for tea plantations and other
fast-growing plantation species, exacerbated by ongoing shifting Hunting as a Threat to Migratory Landbirds
cultivation (Rasul, 2007; Lele and Joshi, 2009); in upland parts The hunting or trapping of wild birds in East and Southeast
of Southeast Asia, expansion of vegetable farms is known to Asia is driven by diverse socioeconomic forces, with considerable
drive deforestation (Poudel et al., 1998). In mainland Southeast variation across the region. Bird trapping to supply the pet trade
Asia and southern China, shifting cultivation has affected large is undoubtedly the leading driver of take in Southeast Asia and
tracts of montane forest landscapes (Fox et al., 2014). It remains parts of China (Dai and Hu, 2017; Harris et al., 2017). It has been
unclear how such extensive land use change (perhaps in synergy implicated in the fast deteriorating status of robins, thrushes,
with climate-change shifts) may impact species using tropical white-eyes, bulbuls, starlings and many other species (Eaton
montane habitats. Anecdotal evidence suggests that montane et al., 2015). Bird trapping has been most severe in Indonesia,
species, including wintering landbirds, may be better adapted to where the practice of keeping pet birds is a well-established
exploit habitat mosaics and successional growth (e.g., Diamond local tradition (Jepson and Ladle, 2005; Nijman, 2010) and it is
and Lovejoy, 1985) and are therefore less sensitive to habitat estimated that 66–84 million individuals of songbirds are kept in
degradation compared to lowland-dependent species. Java alone (Marshall et al., 2020). Although surveys have revealed
The impact of wetland conversion on migratory landbird migratory songbirds, such as Siberian thrush Geokichla sibirica
communities is another major knowledge gap. Until recently, and Siberian rubythroat, in the Southeast Asian pet trade (Yong
only anecdotal observations were available, along with a few et al., 2015; Chng and Eaton, 2016; Chng et al., 2018), the degree
studies from coastal marshes in China and Japan (Ma et al., to which trapping pressures have impacted their populations
2007). Across the floodplains of the major rivers in southern remains unclear.
China, Southeast Asia, Bangladesh and northeast India, most Even less is known about the extent to which migratory raptor
climax wetland vegetation (e.g., seasonally inundated grasslands populations have been impacted by trapping in northern Asia.
and marshland on floodplains) has been heavily modified There is robust evidence that illegal capture in Mongolia, China
and largely replaced by extensive areas of rice paddies, tea and Russia to supply falconry and taxidermy markets outside the
gardens and other agriculture (Round, 2008; Prokop, 2018). Rice region has decimated saker Falco cherrug and other migratory
paddies can support a subset of the migratory bird assemblages falcon populations (Gombobaatar et al., 2004; Lobkov et al., 2011;
associated with freshwater wetlands (Round, 2008; Wong et al., Stretesky et al., 2018). In Russia, several thousand falcons were
2009; Fujioka et al., 2010; Wood et al., 2010). For instance, illegally caught for export in 2012–2016 and trade in falcons
on the Chao Phraya floodplains in central Thailand, the rice increased between 2006 and 2017 (Lobkov et al., 2011; Wyatt,
Frontiers in Ecology and Evolution | www.frontiersin.org 12 April 2021 | Volume 9 | Article 613172Yong et al. Conservation of East Asian Landbirds
2011; Krever and Ivannikova, 2020), despite law enforcement markets selling high volumes of birds have been documented in
efforts. In Southeast Asia, raptors including various migratory Myanmar, Laos, Indonesia and northeast India (Brickle et al.,
species are commonly traded in pet shops or on social media 2008; Bhupathy et al., 2013). Studies of traditional hunting
platforms (Iqbal, 2016; Paridi and Noske, 2017). activities by local people at migration hotspots in China and the
Hunting of wildlife for subsistence and the trade in wild Philippines have also warned of the high number and diversity of
meat and traditional medicines directly threaten a wide range species taken (McClure, 1974; Alonzo-Pasicolan, 1992; Aquino,
of vertebrate species in much of Southeast Asia, the Philippines 1997; Wang et al., 2000). Commercially produced mistnets,
and parts of southern China (Nijman, 2010; Lee et al., 2014; which are now widely available, and improvised fishing nets are
Harrison et al., 2016). Unsustainably high levels of exploitation extensively used in paddy fields and aquaculture areas for both
to supply local, domestic and international demand for wild bird hunting and crop protection (Evans et al., 2000; Gallo-Cajiao
meat have decimated vertebrate fauna and hunting is now et al., 2020). Nets have also been used to reduce bird-strike at
recognized to be a more immediate threat to Southeast Asian airfields (Townshend, 2016b).
vertebrate fauna than deforestation and logging (Tilker et al., In many parts of Southeast and East Asia, the deliberate
2019). Recent work is beginning to unravel the scale and impact release of captive wild animals for religious purposes or ‘merit
of hunting on wild bird populations in Asia (Kamp et al., release’ is well established in Buddhist tradition (McClure,
2015; Gallo-Cajiao et al., 2020), particularly for small migratory 1974; Severinghaus and Chi, 1999; Chan, 2004). Gilbert et al.
songbirds (Box 2). (2012) reported 57 species from bird sellers from Phnom Penh,
In some parts of Southeast Asia, the number of passerines Cambodia alone, with an annual turnover reaching 700,000
taken to supply domestic demand for wild meat is potentially individuals, including large numbers of migratory passerines,
unsustainably high (Evans et al., 2000; Davenport and Heatwole, such as swallows. In Thailand, Cambodia, and Myanmar,
2013), but surprisingly little monitoring exists. Wild meat countries where religious releases are ubiquitous, the cumulative
BOX 2 | The role of trade in the decline of migratory passerines.
The global demand for wildlife for human consumption and the pet trade affects much of the world’s vertebrate biodiversity (Scheffers et al., 2019) and has driven the
unsustainable take of many birds, bringing several species in Asia close to extinction (Sodhi et al., 2004; Eaton et al., 2015; McEvoy et al., 2019). Given that
long-distance migratory passerines tend to build up significant fat stores in preparation for migration (Bairlein, 2002), it is not surprising that such species are targeted
as food by humans. In parts of China and in certain Southeast Asian countries, the illegal capture and trade of small passerines for food occurs at a very large scale
(Kamp et al., 2015). For instance, an estimated 120,000 songbirds were confiscated in Dongli, Tianjin in September 2018 alone (Anon, 2018). In another incident,
poachers made a profit of over 140,000 USD from 510,000 songbirds trapped illegally within 40 days (Wen, 2018). In many instances, birds are kept in flat cages and
are fed chemical agents to be fattened (Li, 2016). Barn swallows are trapped on an industrial scale in northern Laos, exceeding an estimated 100,000 individuals per
year (Evans et al., 2000; Figure 6A). Similarly, thousands of eyebrowed thrushes Turdus obscurus are harvested in parts of Sumatra, Indonesia (Iqbal et al., 2014).
Until the 2000s, the species most traded for food in China was believed to be the yellow-breasted bunting. Since this species has declined catastrophically
(Kamp et al., 2015), poachers appear to have shifted their attention to other species (Heim et al., in press). For example, 33,000 chestnut buntings and 2,000
chestnut-eared buntings Emberiza fucata were confiscated in a single raid in November 2019 in Pingle, Guangxi. Other species often found in ‘fattening centers’
include yellow-browed E. chrysophrys and black-faced bunting E. spodocephala and common rosefinch Carpodacus erythrinus (Let Wild Birds Fly, 2016).
Meanwhile, the pet trade also drives the harvest of large numbers of migratory passerines and raptors. Siberian rubythroats, long-tailed shrikes Lanius schach,
and black-naped orioles Oriolus chinensis are among the more commonly traded species. Surveillance work has revealed a diversity of passerines, including
thrushes, starlings, flycatchers and raptors being trapped in the wild and sold in pet bird shops from Vietnam to Indonesia (Iqbal, 2016; Chng et al., 2018;
Figure 6B).
Amidst increasing efforts to tackle bird hunting, better monitoring of the vast trade in migratory birds across Asian countries is urgently required. There is a need,
(1) to analyze whether the levels of illegal (and legal) hunting are sustainable and, (2) to assess if ongoing hunting could lead to further population declines, as already
shown for some migratory taxa, such as waders (Gallo-Cajiao et al., 2020).
FIGURE 6 | Migratory landbirds are heavily hunted in Southeast Asia and parts of China for the pet trade, and for food. (A) Grey-faced buzzard Butastur indicus for
sale at a pet shop, (B) various swallow species are caught in large numbers for human consumption in northern Laos (Image credits: Yong Ding Li).
Frontiers in Ecology and Evolution | www.frontiersin.org 13 April 2021 | Volume 9 | Article 613172Yong et al. Conservation of East Asian Landbirds
impact of merit release on migratory landbird populations is light (Zhao et al., 2020) to attract birds, which have increased the
likely to exceed many millions of swallows, wagtails, reed warblers number of birds ringed during migration.
and other small passerines. While most individuals will be Light-level geolocators (Aoki et al., 2020; Heim et al., 2020),
released back to the wild, release often occurs in unsuitable collaborative tracking network systems, such as the Motus
habitat and high mortalities during transport and capture can be automated radio telemetry arrays (Taylor et al., 2017) and GPS-
expected (Clewley et al., 2018). based tracking systems may all offer cost-effective means to fill
Drawing from diverse sources, we found evidence of trapping knowledge gaps on the migration and distributions of landbird
or trade for at least 180 of the over 380 migratory landbird species, migrants in the EAF. These methods may be complemented
representing nearly half (47%) of all species in the EAF (see by molecular approaches (Seki and Ogura, 2007; Aoki et al.,
Supplementary Table 2). The actual number of species involved 2020) and intrinsic markers, such as stable isotope signatures in
is likely to be much higher, given that market and community tissues (Choi and Nam, 2011; Choi et al., 2020b). For instance,
surveys typically fail to identify many individuals to species, genetic markers have been used to infer the breeding areas of
especially leaf-warblers, white-eyes and other difficult groups migrating Ryukyu robins Larvivora komadori (Seki and Ogura,
(Rentschlar et al., 2018). In several families (cuckoo-shrikes, 2007). Stable isotopes from feathers have been used to link
pigeons and doves, drongos, starlings and buntings) almost all breeding and non-breeding areas (Choi and Nam, 2011; De Jong
migratory species are affected by some level of trapping or trade et al., 2019) and to determine migration patterns (e.g., leap-
in the region, whereas other families (swifts and accentors) seem frog versus chain migration; Weng et al., 2014; Choi et al.,
to be unaffected. 2020b). Stable isotope analysis can also provide missing data
on the diets and molting patterns of migratory birds during
stopover. Despite this, some challenges remain. For instance, no
calibration algorithm between precipitation and feather isotope
KNOWLEDGE GAPS values is available for Asian landbirds (Choi et al., 2020b). Broad
Various knowledge gaps hinder our present understanding of longitudinal similarities of hydrogen isotope ratios across Siberia
many aspects of landbird migration in the EAF. The basic ecology make it difficult to pinpoint precise breeding areas for some
of many landbirds, their migratory routes and conservation species (Choi and Nam, 2011; De Jong et al., 2019) and stable
status, as well as the key threats and causes of decline still isotope ratios may also be influenced by feeding habitats and
require study (re-worded due to poor structure). The increasing environmental pollutants (Sun et al., 2012).
availability of novel tools to track migration is rapidly improving
the situation. Unlike in Europe and North America, the lack Gaps in Knowledge of Species Ecology
of systematic, large-scale monitoring schemes with coordinated
data collection across most parts of Asia means that it is difficult and Natural History
to determine broad population trends for migratory species. Compared to other flyways, the ecology of migratory landbirds
There is, however, a potential for citizen science to fill such gaps in in non-breeding areas in the Asian tropics remains poorly
the coming decades (Tulloch et al., 2013a,b), and there are already understood (Newton, 2010; McKinnon and Love, 2018). For
good precedents from the region, especially in Japan and Taiwan instance, the rufous-headed robin Larvivora ruficeps is relatively
(Lin and Pursner, 2020; Japan Bird Research Association, 2021). well-documented at its breeding ground in central China (Zhao
et al., 2017), but its wintering distribution in the tropics was
entirely putative (Medway and Wells, 1976; Nisbet, 1976) until
Gaps in Knowledge of Migratory Routes recent observations (Lim et al., 2020). In another example, the
and Connectivity streaked reed warbler is on the verge of extinction, yet its breeding
Data on migratory routes are now available for some raptors distribution remains largely undetermined (Round and Allen,
and larger songbirds (Figure 2 and Table 2). Apart from the 2010; Allen, 2020). Similarly, until recently, movements of most
studies of the eastern populations of some wide-ranging species, migratory raptors in Southeast Asia were known only through
conducted by Japanese and Korean researchers, surprisingly direct observations at bottleneck sites in northern Vietnam, the
few small Siberian passerines have been tracked (Heim et al., Thai-Malay Peninsula, the Greater Sundas and the Philippines
2020). Large knowledge gaps remain for owls, nightjars, rollers, (Tordoff, 2002; Nijman et al., 2006; Germi et al., 2009). Tracking
doves, and many passerines, including most thrushes, flycatchers studies (Higuchi et al., 2005; Shiu et al., 2006) have substantially
and leaf-warblers. Tracking the migratory routes of particular improved understanding of the movements and ecology of some
species and populations has been instrumental in improving our species, such as the Oriental honey buzzard. The wintering
understanding the migration ecology and survival of landbirds. ecology of most raptors, however, remains scarcely studied (but
There are ample opportunities for continued work to identify see Syartinilia et al., 2015).
routes under threat, geographical connectivity, habitat use and Furthermore, there are significant gaps in knowledge on how
key stopover areas, all of which have direct implications for habitat conversion, loss and degradation impact assemblages of
conservation (Runge et al., 2014; McKinnon and Love, 2018). migratory landbirds in forests, cultivated areas and freshwater
Indeed, several projects have been established to track the wetlands, especially at their wintering grounds. A better
migration of some species (Townshend, 2019) aided by novel field understanding of the ecological traits of a species, such as age
techniques, such as the use of sound (Senda et al., 2018) and blue at first breeding, clutch size, survival and life history, migration
Frontiers in Ecology and Evolution | www.frontiersin.org 14 April 2021 | Volume 9 | Article 613172You can also read
